ABSTRACT Field studies have identified that male-biased infection can lead to increased rates of transmission, so we examined the relative importance of host sex on the transmission of a trophically transmitted parasite (Pterygodermatites peromysci) where there is no sex-biased infection. We experimentally reduced infection levels in either male or female white-footed mice (Peromyscus leucopus) on independent trapping grids with an anthelmintic and recorded subsequent infection levels in the intermediate host, the camel cricket (Ceuthophilus pallidipes). We found that anthelmintic treatment significantly reduced the prevalence of infection among crickets in both treatment groups compared with the control, and at a rate proportional to the number of mice de-wormed, indicating prevalence was not affected by the sex of the shedding definitive host. In contrast, parasite abundance in crickets was higher on the grids where females were treated compared with the grids where males were treated. These findings indicate that male hosts contribute disproportionately more infective stages to the environment and may therefore be responsible for the majority of parasite transmission even when there is no discernable sex-biased infection. We also investigated whether variation in nematode length between male and female hosts could account for this male-biased infectivity, but found no evidence to support that hypothesis.

[Show abstract][Hide abstract]ABSTRACT:
Male-bias in parasite infection exists in a variety of host – parasite systems, but the epidemiological importance of males and, specifi cally, whether males are responsible for producing a disproportionate amount of onward transmission events (male- biased transmission) has seldom been tested. Th e primary goal of our study was to experimentally test for male-biased transmission in a system with no sex-biased prevalence. We performed a longitudinal fi eld experiment and continuously removed intestinal nematode parasites from either male or female white-footed mice and recorded the subsequent transmis- sion among the untreated sex. We predicted males are responsible for the majority of transmission and female mice would have lower infection prevalence under the male-anthelmintic treatment than controls and that male mice would experience little or no change in infection prevalence under female-anthelmintic treatment compared to controls. Our second goal was to evaluate physiological hypotheses relating to the mechanisms that could generate the observed transmission pattern. To that end, we examined a cross-sectional sample of hosts to explicitly test for diff erences in parasite intensity, parasite egg shedding rate and reproductive output per parasite between male and female hosts. Removing parasites from male mice resulted in lower infection rates among female mice but, in contrast, there was no eff ect of female-deworming on infection rates among male mice; providing evidence that males provide disproportionately greater numbers of transmission events than females. We found no diff erence in prevalence, intensity, or fecundity of parasites between sexes in the cross-sectional sample of mice and rejected the mechanistic hypotheses. Without male-biased prevalence, intensity, or parasite fecundity, we concluded that male-biased transmission is unlikely to be created via physiological diff erences and the parsimonious explanation is that male behavior spreads infective stages in a more successful manner. We demonstrate that transmission heterogeneities can exist in the absence of individual heterogeneities in infection.

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Many parasites with complex life cycles are known to modify their host phenotype to enhance transmission from the intermediate host to the definitive host. Several earlier studies explored these effects in acanthocephalan and trematode parasites, especially in aquatic ecosystems; however, much less is known about parasite‐mediated alterations of host behavior in terrestrial systems involving nematodes. Here, we address this gap by investigating a trophically transmitted nematode (Pterygodermatites peromysci) that uses a camel cricket (Ceuthophilus pallidipes) as the intermediate host before transmission to the final host, the white‐footed mouse (Peromyscus leucopus). In a laboratory experiment, we quantified the anti‐predatory responses of the cricket intermediate host using simulated predator cues. Results showed a decrease in jumping performance among infected crickets as compared with uninfected crickets, specifically in terms of frequency of jumps and jumping distance. Additionally, the relationship between parasite load and frequency of jumps is negatively correlated with the intensity of infection. These behavioral modifications are likely to increase vulnerability to predation by the definitive host. An analysis of the age‐intensity pattern of infection in natural cricket populations appears to support this hypothesis: parasites accumulate with age, peak at an intermediate age class before the intensity of infection decreases in older age groups. We suggest that older, heavily infected crickets are preferentially removed from the population by predators because of increased vulnerability. These results show that cricket intermediate hosts infected with P. peromysci have diminished jumping performance, which is likely to impair their anti‐predatory behavior and potentially facilitate parasite transmission.

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SUMMARY We investigated offspring quality in fleas (Xenopsylla ramesis) feeding on non-reproducing, pregnant or lactating rodents (Meriones crassus) and asked whether (a) quality of flea offspring differs dependent on host reproductive status; (b) fleas trade off offspring quantity for quality; and (c) quality variables are inter-correlated. Emergence success was highest when parents exploited pregnant hosts, while development time was longest when parents exploited lactating hosts. Male offspring from fleas fed on non-reproductive and pregnant hosts were larger than those from lactating hosts whereas female offspring from fleas fed on pregnant hosts were larger than those from both lactating and non-reproductive hosts. Male offspring survived under starvation the longest when their parents exploited lactating hosts and the shortest when their parents exploited pregnant hosts. Female offspring of parents that exploited lactating hosts survived under starvation longer than those that exploited non-reproductive and pregnant hosts. Emergence success and development time decreased as mean number of eggs laid by mothers increased. Fleas that were larger and took longer to develop lived significantly longer under starvation. These results indicate the presence of a trade-off between offspring quantity and quality in fleas exploiting female Sundevall's jird in varying reproductive condition but this trade-off depended on the quality trait considered.

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Male hosts are responsible for the transmission of a trophically transmitted parasite,Pterygodermatites peromysci, to the intermediate host in the absence ofsex-biased infectionLien T. Luong*, Daniel A. Grear, Peter J. HudsonCenter for Infectious Disease Dynamics, Department of Biology, 208 Mueller Laboratory, The Pennsylvania State University, University Park, PA 16802, USAa r t i c l e i n f oArticle history:Received 13 March 2009Received in revised form 30 March 2009Accepted 31 March 2009Keywords:Male-biased parasitismSex-biased transmissionIndirect life cyclePeromyscusWhite-footed mouseCamel cricketa b s t r a c tField studies have identified that male-biased infection can lead to increased rates of transmission, so weexamined the relative importance of host sex on the transmission of a trophically transmitted parasite(Pterygodermatites peromysci) where there is no sex-biased infection. We experimentally reduced infec-tion levels in either male or female white-footed mice (Peromyscus leucopus) on independent trappinggrids with an anthelmintic and recorded subsequent infection levels in the intermediate host, the camelcricket (Ceuthophilus pallidipes). We found that anthelmintic treatment significantly reduced the preva-lence of infection among crickets in both treatment groups compared with the control, and at a rate pro-portional to the number of mice de-wormed, indicating prevalence was not affected by the sex of theshedding definitive host. In contrast, parasite abundance in crickets was higher on the grids wherefemales were treated compared with the grids where males were treated. These findings indicate thatmale hosts contribute disproportionately more infective stages to the environment and may thereforebe responsible for the majority of parasite transmission even when there is no discernable sex-biasedinfection. We also investigated whether variation in nematode length between male and female hostscould account for this male-biased infectivity, but found no evidence to support that hypothesis.? 2009 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.1. IntroductionA number of studies have found that the majority of parasitetransmission events can be attributed to a minority of infectedhosts such that specific functional groups serve as the primaryshedders of infective stages (Anderson and May, 1991; Woolhouseet al., 1997; Perkins et al., 2003; Ferrari et al., 2004; Lloyd-Smithet al., 2005). Comparative studies have demonstrated that malesare more likely to be infected than females and tend to carry higherparasite intensities, particularly nematode infections of mammals(Poulin, 1996a; Schalk and Forbes, 1997; Moore and Wilson,2002). However, while a male bias in parasitism appears to impli-cate male hosts in driving the parasite dynamics, some have ar-gued that the sex bias is often relatively small (<5%) and that thismay not be epidemiologically important (Wilson et al., 2002).Evidence of between-host heterogeneity in transmission hasbeen documented in only a handful of host–parasite systems. Per-kins et al. (2003) measured the number of potential transmissionevents of tick-borne encephalitis by recording the distribution ofco-feeding on yellow-necked mice (Apodemus flavicollis) and foundthat the sexually active males of high body mass were responsiblefor more than 90% of the transmission potential. In an experimen-tal study, Ferrari et al. (2004) treated either male or female yellow-necked mice with an anthelmintic to remove the most commonnematode, Heligmosomoides polygyrus, and found that when maleswere treated, the level of infection amongst the untreated femalesfell, but in sites where females were treated the prevalence ofinfection among males remained unchanged. Both of these studiesconcluded that male hosts were primarily responsible for drivingparasite transmission but there was also evidence of sex-biasedinfection; males were more likely to be infected and had higherintensities of infection. While these studies show that sex-biasedinfection is epidemiologically important they do not tell us if thefindings were simply a consequence of higher susceptibility inthe males or whether the male infectivity per parasite was alsogreater.Even in the absence of sex-biased infection, males could still beimportant if they simply shed more infective stages and/or thosestages are more likely to result in an infection. Variations in thetransmission process can be generated by any one or a combina-tion of processes: (i) differential production of infective stages,(ii) differential survival of free living stages, (iii) differential expo-sure to infective stages, and (iv) differential establishment of para-sites (Anderson and May, 1991; Keeling et al., 2001). Therefore,sex-biased transmission can arise if intrinsic differences between0020-7519/$36.00 ? 2009 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.doi:10.1016/j.ijpara.2009.03.007* Corresponding author. Tel.: +1 814 865 0522; fax: +1 814 865 9131.E-mail address: ltl1@psu.edu (L.T. Luong).International Journal for Parasitology 39 (2009) 1263–1268Contents lists available at ScienceDirectInternational Journal for Parasitologyjournal homepage: www.elsevier.com/locate/ijpara

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male and female hosts lead to variation in infectivity (via mecha-nisms i and ii) independently of sex-biased parasitism (via mecha-nisms iii and iv).Among helminth infections, variation in infectivity per host is aproduct of the number of parasites and egg output per parasite(Michel, 1969; Ractliffe and LeJambre, 1971; Stear et al., 1997).Moreover, intrinsic differences between hosts can not only influ-ence the probability of parasite establishment, but also helminthgrowth, survival, size and consequently per capita fecundity (Key-mer and Slater, 1987; Stear et al., 1995, 1997; Poulin, 1996b;Tompkins and Hudson, 1999; Wilkes et al., 2004). Consequently,hosts that harbour larger, more fecund worms should exhibit rela-tively high shedding rates and hence contribute more infectivestages to the environment than those hosts that carry smallerand less fecund worms. In this way, shedding rates can vary be-tween functional host groups even if worm intensity does not. Thisleads to the question, ‘Can differences in infectivity between sexesexist in the absence of sex-biased infection?’.We address this question by using a parasite–host system withno male bias in infection and a random distribution of parasites(Fig. 1; Vandegrift and Hudson, in press). We focus on the white-footed mouse (Peromyscus leucopus) and its trophically transmittednematode, Pterygodermatites peromysci. Since the parasite has acomplex life cycle, we use the intermediate host, a camel cricket(Ceuthophilus pallidipes) as a means of sampling infective stagesin the environment. This approach provides an alternative to theconventional egg per gram (EPG) of faeces method of measuringhost infectivity. One drawback of EPG data is that not all eggs shedinto the environment are fertile or have the potential to be infec-tive (Keymer and Anderson, 1979; Keymer, 1982; Bush et al.,2001; Hansen et al., 2004) and second, variation in exposure andsusceptibility between male and female hosts can contribute addi-tional variation to the transmission process. We circumvent theseconfounding factors by using the intermediate host as a proxy forinfectivity of the definitive host. Although the crickets may exhibitvariation in exposure and/or susceptibility, this individual-levelheterogeneity is not expected to manifest at the population levelwhere we estimate infectivity and it is therefore unlikely to influ-ence the outcome of our experiment.We test the hypothesis that heterogeneities in parasite trans-mission, in the form of male-biased infectivity, can arise indepen-dently of differential establishment rate by experimentallymanipulating the levels of infection in either male or female hosts.We selectively reduced the number of definitive hosts sheddinginfective eggs into the environment, and estimated infectivity asthe level of infection in the camel cricket. If parasite recruitmentrate in crickets is not influenced by host sex, but simply by theavailability of infected hosts (shedders) in the population, we ex-pect the level of infection among crickets in either treatment groupto be lower compared with the untreated control group, but notsignificantly different from each other. In particular, we predictthat the infection levels will be reduced at a rate proportional tothe number of mice treated in the population, independent of thesex we treated. Alternatively, if infectivity is sex-biased such thatmale hosts are more effective at shedding and/or disseminatinginfective stages than female hosts, we predict lower levels of infec-tion among crickets collected from areas where males were treatedcompared with where females were treated.In addition, we examined a potential mechanism underlying thebetween-host variation in infectivity by quantifying the variationin mean nematode length between male and female hosts. A majorcomponent of parasite transmission is the rate at which infectivestages such as eggs are shed into the environment. Intrinsic differ-ences between individual hosts can influence parasite survival,developmental, growth and fecundity (Poulin, 1996b; Patersonand Viney, 2002). Furthermore, numerous studies have demon-strated that nematode fecundity is positively correlated with nem-atode size (Ractliffe and LeJambre, 1971; Michael and Bundy, 1989;Skorping et al., 1991 Stear et al., 1995, 1997; Tompkins and Hud-son, 1999). Consequently, some hosts may harbour relativelysmall, less fecund nematodes while others harbour larger and morefecund nematodes, potentially generating variation in sheddingrates and hence infectivity. If variation in nematode size accountsfor male-biased infectivity, we would expect male hosts to harbourlarger nematodes than female hosts.2. Materials and methods2.1. Study systemThe gastrointestinal nematode P. peromysci infects the smallintestine of the white-footed mouse (P. leucopus) and has a 5-weekpre-patent period (Luong, unpublished data; also see Oswald,1958b). Parasite eggs pass into the host faeces and are ingestedby the intermediate host, the camel cricket (C. pallidipes). The L1hatches in the midgut, penetrates the hemocoel and develops toan encysted infective L3 over a period of 10–12 days (Oswald,1958a). Susceptible mice become infected when they ingest crick-ets harbouring infective cysts (Oswald, 1958b; O’Brien and Etges,1981). Cricket eggs hatch in late summer and early instar nymphsover-winter to become the next years breeding adults, which ma-ture in late summer (Lavoie et al., 2007).2.2. Trapping and treating miceA total of nine trapping grids were established in open hard-wood forests of central Pennsylvania. Each grid was separated bya minimum of 200 m, a sufficient distance given that mice wererarely observed moving between adjacent grids. Of the 870 cap-tures, only four mice moved between adjacent grids and were re-corded for a maximum of two consecutive trap nights beforesettling on a different grid for the remainder of their captures. Eachgrid consisted of 64 multi-capture live traps (Ugglan, Graham,Sweden) located at 10 m intervals in a 8 ? 8 linear configuration.Fig. 1. The relationship between log variance and log mean of parasite (Pterygo-dermatites peromysci) abundance for adult mice on the four extensive trapping sitesfor each year from 2003 to 2007. The dotted line represents the 1:1 relationshipwhere the variance equals the mean, as expected for a random distribution, and thesolid line is the fitted regression line weighted for sample size (modified fromVandegrift and Hudson, in press).1264L.T. Luong et al./International Journal for Parasitology 39 (2009) 1263–1268

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Grids were checked for 2 consecutive days every other week fromApril 29 to September 10, 2008, totalling 10 trapping sessions forall grids. Individual mice were tagged with a s.c. passive inducedtransponder for individual identification (TrovanTM, EIDAP, Alberta,Canada). In three replicate grids, males alone received an anthel-mintic treatment, on three other replicate grids females receivedtreatment, and on three control grids no mice were treated. Trea-ted mice were orally administered 1 ll/g of Levamisole Hydrochlo-ride (dose: 36 mg/kg, AgriLabs?, Missouri, USA) on the thirdtrapping session and again at each subsequent capture; controlmice were given sterilized water. A preliminary experiment wasconducted during the summer of 2007 to verify the efficacy ofthe anthelmintic drug, which was shown to be effective for at least2 weeks, but for no longer than 4 weeks. Hence, treating mice inthe present study every 2 weeks should be sufficient to preventinfection (Luong, unpublished data). This experiment was con-ducted with the approval of the Pennsylvania State Animal CareCommittee (IACUC #23268, ‘‘Transmission Dynamics of Diseasein Wildlife Reservoir Hosts”).2.3. Transmission to the intermediate hostCamel crickets (C. pallidipes) were collected using pitfall trapslocated in close proximity to every other mouse trap, and on alter-nating rows of each grid (total = 16 traps/grid). The pitfall trapswere set and checked on the same schedule as the mouse trappingsessions. During the months of August and September, we aug-mented our collection effort by setting bait (oatmeal flakes) trailsadjacent to the mouse traps and collecting crickets from the bait.Note there was no significant difference in infection prevalencefor crickets collected in pitfalls versus bait trails (Fisher’s Exacttest, two-tailed, P > 0.05). Prevalence of infection was calculatedas the number of infected crickets divided by the total number dis-sected. The parasite abundance for a treatment group was mea-sured as the total number of cysts recovered divided by the totalnumber of crickets collected, including uninfected individuals.The developmental stage and caudal femur length (estimate ofbody size) of each cricket were also recorded.To verify that the cysts were P. peromysci larvae, a representa-tive sample of infective cysts were fed to 22 laboratory white-footed mice. After a 4–6 week period of development, mice werenecropsied and worms were identified as P. peromysci based onmorphological characteristics.2.4. Nematode lengthSince animals from the present study could not be sampleddestructively, adult stages of the nematode were obtained fromnecropsies of animals collected at the end of various unrelated fieldexperiments conducted between 2003 and 2007 between themonths of August and October; only nematodes recovered fromhosts in control groups from previous experiments were included.Upon dissection, nematodes were immediately transferred to andstored in a preservative of 90% ethanol and 10% glycerol. Individualnematodes were photographed under a stereomicroscope (Leica?S6E) with a digital camera (Nikon?Coolpix 4500); nematodelength was then measured with the ImageJ software package.2.5. Statistical analysesStatistical analyses were performed in R (www.r-project.org). Ageneralized linear model (GLM) with binomial errors was used toanalyze parasite prevalence among treatment and control groups.Differences in parasite abundance were analyzed with negativebinomial errors. Explanatory variables included cricket size, trap-ping month, grid and anthelmintic treatment. Significance levelswere based on the deviance explained by each factor followingstepwise deletion, retaining variables with P < 0.05 based on v2-statistics. An a posteriori Helmert contrast was employed to testfor differences between specific treatment groups. We calculatedthe expected level of infection based on the proportion of micetreated in the grids, i.e., assuming no sex-biased transmission.Forexample, theexpectedgrids = (proportion infection of control) ? (proportion infection ofcontrol) ? (proportion males treated), and so on for infection prev-alence in female-treated grids. The expected mean parasite abun-dance in each treatment group was calculated in a similarmanner; this value was then used to generate a distribution ofthe expected number of cysts per cricket, based on a Poisson distri-bution. Although the predictions of this experiment are directional,we use two-tailed tests throughout. Nematode lengths were com-pared between host sexes using a generalized linear model with aPoisson error structure. Fixed host factors included body mass, sexand intensity of infection (number of nematodes per infected host).prevalence formale-treated3. Results3.1. Anthelmintic treatment of miceWe caught 870 white-footed mice over the course of 200 trapnights and if a mouse was re-caught during a subsequent trap ses-sion then it was defined a resident. A total of 67 resident mice werecaptured on the control grids. On the female-treated grids, a totalof 70 resident mice were caught and tagged, of these 33 females(47.1%) received the anthelmintic treatment. On the male-treatedgrids, 36 males out of the 65 (55.4%) resident mice were treated.3.2. Prevalence of infection in the intermediate hostThe prevalence of infection was not significantly different be-tween the treatment and control grids prior to treatment, i.e., forthe month of May (deviance (=sum of squares) = 2.26, degrees offreedom (D.F.) = 2, P = 0.32). Anthelmintic treatment of the defini-tive host reduced the prevalence of infection among crickets inthe manipulated grids (Fig. 2a). The analysis on prevalence of infec-tion in crickets post-treatment (June–September) revealed a signif-icant effect of the anthelmintic treatment (minimal model,deviance = 8.47, D.F. = 2, P = 0.01) and month (deviance = 32.3,D.F. = 1, P < 0.001), all other factors and interactions were not sig-nificant. The prevalence of infected crickets was higher in the con-trol grids (% mean ± standard error (SE) = 12.5 ± 2.0%) than eitherthe female-treated (% mean ± SE = 7.4% ± 1.5%) or the male-treated(6.4 ± 1.5%) grids. Given the significance of month, further analyseswere performed for the months of August and September.Although we did not detect a significant effect of the anthelminticon cricket infection prevalence in August (deviance = 3.40, D.F. = 2,P = 0.18), the anthelmintic treatment did have a significant effect inSeptember (deviance = 8.26, D.F. = 2, P = 0.02) in that, the preva-lence of infection in crickets was significantly higher in the controlgridsthan either the female-treated(coeff.) = ?1.41, SE = 0.61, z = ?2.32, P = 0.02) or male-treated grids(coeff. = ?1.82, SE = 0.74, z = ?2.48, P = 0.01). An a posteriori com-parison of the prevalence of infection between the treated gridsshowed no significant difference between the two treatmentgroups (coeff. = ?0.60, z = ?1.44, P = 0.15).To account for differences in the proportion of the mouse pop-ulation treated on the female-treated (47.1%) and male-treatedgrids (55.4%), we compared the observed levels of infection amongcrickets with the expected values for September and found that therelative reduction in infection corresponded closely to the propor-tion of mice de-wormed in each treatment group (Table 1). The(estimate coefficientL.T. Luong et al./International Journal for Parasitology 39 (2009) 1263–12681265

The prevalence of infection in the crickets was reduced in bothtreatment groups to a level that was proportional to the numberof hosts shedding and there was no difference based on whethermales or females were responsible for the shedding. When femalesserved as the main shedders of parasite eggs, parasite abundanceamong the crickets was significantly lower than when malesserved as the primary shedders, indicating that males are indeedresponsible for more transmission than females. The higher para-site abundance among the grids with the males shedding wasdue primarily to a few heavily infected crickets, suggesting thatmales are contributing disproportionately more infective stagesthan females. Overall our results provide evidence to support thehypothesis that there is male-biased parasite transmission in a sys-tem with no male bias in infection and a random distribution ofparasites.Our finding of sex-biased transmission is consistent with anexperimental study by Ferrari et al. (2004) where authors demon-strated that male mice were driving the transmission of an intesti-nal nematode. However our results go further in three distinctways. Firstly, Ferrari et al. (2004) recorded prevalence in the sus-ceptible host to test for sex-biased transmission and yet individualvariation in exposure and susceptibility, especially between thesexes, can contribute additional variation to the transmission pro-cess. We bypassed this confounding factor to some extent byfocusing on a parasite with a complex life cycle and used the inter-mediate host as a proxy for infectivity (i.e., shedding rate of in-fected host). Although the cricket host may present its own set oftransmission barriers arising from individual variation in exposureand/or susceptibility, this individual-level heterogeneity shouldnot be apparent at the population level of the crickets where wedo the estimation. Second, Ferrari et al. (2004) examined a systemwhere there was sex-biased parasitism to begin with and so it wasnot clear if the sex-biased transmission was simply a consequenceof the variation in the sex-biased parasitism or whether maleswere responsible for more infection. Third, the parasite was aggre-gated in the host population and the individuals in the tail of thedistribution were primarily males and it may be that the individu-als in the tail are important for driving the infection.A possible limitation in our study is the sampling method forthe intermediate host in that pitfall traps and bait trails tend tobe biased towards animals that are active. There is also a possibil-ity that infected crickets experience reduced activity relative touninfected crickets; if so we may have underestimated the levelof infection among crickets. Such a sampling bias, however, wouldsuggest that our findings actually err on the conservative side. Also,the same method was applied consistently across all treatmentgroups and should therefore not influence the differences observedbetween the treatment groups. A second possible concern is thatlocal environmental conditions (e.g., humidity and temperature)may vary between grids and potentially influence the infectivityof the eggs to the intermediate host. Yet our analyses show thatgrid and its interaction with treatment were not significant factorsin the statistical models; hence there was no evidence of any sys-tematic bias between the grids.Due to the random distribution of parasites per definitive hostin this study system (Vandegrift and Hudson, in press), we can ruleout mechanisms that produce differential exposure and suscepti-bility in the definitive host as a source of sex-biased infectivity.However, physiological factors such as immune response can con-ceivably give rise to differences in infectivity, for instance if malehosts harboured larger helminth parasites than female hosts (Pou-lin, 1996b). However we found no evidence to support this hypoth-esis; the mean nematode length was comparable for male andfemale hosts. Still, other factors such as duration of egg shedding,behavioural differences, and variation in contact rates betweenmale and female hosts may also generate a male bias in infectivity.Further research is needed to understand the mechanism(s) under-lying the heterogeneity in infectivity.Few studies have reported on the infection level of the interme-diate host following anthelmintic treatment of the definitive host;further, our study is the first that we are aware of to do so by selec-tively treating male and female hosts. Parr and Gray (2000) re-ported a significant reduction in the prevalence of Fasciolahepatica in snails when all the definitive hosts were de-wormed.Similarly, an urban baiting experiment showed that the proportionof vole intermediate hosts infected with Echinococcus multiloculariswas lower in areas where foxes of both sexes received an anthel-mintic treatment compared with untreated areas (Hegglin et al.,2003). Sampling the intermediate host not only provides a rela-tively easy method for assessing the efficacy of an anthelmintictreatment; it also allows for successive data collection essentialfor understanding the temporal dynamics of parasitism, informa-tion that would otherwise be lost in the destructive sampling ofdefinitive hosts. Consequently, we found evidence that the effectof the treatment increased with time, implying a time lag in the re-sponse of crickets to the anthelmintic treatment. This may havebeen a consequence of the extrinsic incubation period, accumula-tion of cysts in individual crickets over time, ontogenetic changesin the feeding habits of the crickets, and/or seasonal changes inthe cricket population. Further work is needed to identify the rela-tive importance of these mechanisms in generating potential sea-sonal dynamics in the parasite transmission process (Vandegriftand Hudson, in press).In conclusion, we experimentally demonstrated a male bias inthe infectivity of a trophically transmitted parasite, notwithstand-ing a random parasite aggregation and lack of sex-biased parasit-ism in the definitive host population. These results suggest thatvariation in host infectivity can arise independently of differentialexposure and susceptibility mechanisms that underlie sex-biasedparasitism. Importantly, male definitive hosts appeared to be dis-proportionately more responsible for the majority of transmissionto the intermediate host. Identifying the functional group respon-sible for transmission is not only useful for understanding parasitetransmission dynamics, but is also informative for targeting thevulnerable host groups in disease intervention programs (Wool-house et al., 1997). Sex-biased parasite transmission can also havepotentially important evolutionary implications as a result of dif-ferential selection pressures on males and females. For instance,Fig. 3. Frequency distribution of Pterygodermatites peromysci cysts in the interme-diate cricket host (Ceuthophilus pallidipes) collected from control (black), female-treated (gray) and male-treated (hatched) grids. Uninfected crickets (n = 751) wereexcluded for ease of interpretation.L.T. Luong et al./International Journal for Parasitology 39 (2009) 1263–12681267